The Relationship Between Owner and Dog Anxiety

April 29, 2020

While operating CPT for the past 30 years I have availed myself of many anecdotal observations. One of the more intriguing impressions is the apparent correlation between anxious owners and dogs exhibiting anxiety, aggressive behavior, or both. Therefore, I eagerly read recent research from the University of Ljubljana.

I. A Thought Provoking Research Paper

The paper, “Dogs’ Sociability, Owners Neuroticism, and Attachment Style to Pets as Predictors of Dog Aggression,” was published on February 18, 2020 in the journal Animals. The authors are Elena Gobbo and Manja Zupan from the Department of Animal Science at the University of Ljubljana in Slovenia. Gobbo and Zuppan evaluated associations between owner personality types and attachment styles and their dogs’ behavior. The overall finding is that owners who are neurotic, emotionally disconnected, less controlling, or less structured are more likely to possess dogs exhibiting aggressive behavior.

In addition, their research provided other pertinent results. The study found that dogs exhibiting aggression to humans tend to be less social with unfamiliar humans than are non-aggressive dogs. More saliently, there is a clear inter-relationship between dog-human aggression, dog-dog aggression, and owner neuroticism. Thus, dogs exhibiting aggression to humans are also more likely to exhibit aggression to dogs than are dogs non-aggressive to humans. Similarly, there is a disproportionate probability that an anxious person will own a dog-aggressive or human-aggressive dog.

Interestingly, the study correlated another characteristic germane to deleterious outcomes. Persons displaying an avoidant attachment style are more likely to reside with dogs exhibiting dog-owner aggression. Furthermore, somewhat ironically, persons with an avoidant attachment style are more likely to own dogs exhibiting separation distress. Therefore, dogs owned by avoidant persons are not only more likely to act aggressively toward the owner, but also more likely to become distressed upon the owner’s departure.

Of the owner personality traits studied (agreeableness, conscientiousness, extraversion, neuroticism, and openness), only neuroticism had a significant effect on the dog-human and dog-dog aggressive propensity of the pet.[1] However, the study never answered why. What is the chicken and egg?

Do neurotic and avoidant owners make their dogs anxious? Do neurotic dogs make their owners anxious? Do neurotic owners purposefully acquire anxious dogs that mirror the owner’s personality type? Or are all the preceding causations true?

IIa. Do Neurotic and Avoidant Owners Make Their Dogs Anxious?: Human Personality Types

Understanding human neuroticism is the first step in comprehending the mutual interaction between human and dog emotional states. The “Big 5 “human personality types (agreeableness, conscientiousness, extraversion, neuroticism, and openness)[2]were formally classified in 1993 by Lewis Goldberg,[3]a University of Oregon psychology professor, after he advanced work begun by Ernest Tupes and Raymond Christal in the 1960s and John Digman in the early 1990s.[4] In the model, neuroticism is defined as a proclivity to exhibit distress and negative emotions, such as fear, sadness, anger, anxiety, irritability, loneliness, worry, self-consciousness, dissatisfaction, hostility, shyness, low self-confidence, and vulnerability,[5]whereupon the person exhibits nervousness, has low tolerance for stress or aversive situations or stimuli, and displays emotionally instability.[6]

The following video explains the Big 5 personality types defined by Goldberg:

Now that we comprehend the definition of neuroticism and can envision practical applications where neuroticism is maladaptive, let’s consider why and how a neurotic owner can transmit his/her neurotic tendencies to a household dog. The answer lies in the psychological principals of emotional contagion.

Emotional contagion is the phenomenon of having one person’s emotions and related behaviors directly trigger similar emotions and behaviors in other people.[7] Emotional contagion is a basic form of empathy that makes individuals able to experience others’ emotions. Emotional contagion can be linked to facial mimicry and body language. The stronger the social bond the higher the level of mimicry. Social mimicry is present in dogs, humans, and other primates.[8]

Applying the preceding, both people and dogs exhibit the phenomenon of emotional contagion; owners and dogs typically have a close social and emotional bond; and humans and dogs in many respects communicate similarly, whereupon they readily understand each other’s verbal, facial, and body communications. Consequently, the logical conclusion is that human owners exhibiting a neurotic emotional state or neurotic behavior may infect their dogs with homologous state anxiety and concomitant anxiety-related behaviors.

Moreover, the power of emotional contagion is not exclusive to neuroticism. A study found significant positive correlations between owners and their dogs in all 5 personality dimensions (neuroticism, extraversion, conscientiousness, agreeableness, and openness). This similarity could not be attributed solely to the owner’s self-projection, since the similarity in the first four dimensions was also significant when an independent peer person assessed the dog. The analysis provides evidence that dogs resemble their owners.[9]

Part of the above effect is likely attributable to similar-attachment theory, which we will discuss later. However, there are also acute and chronic environmental components attributable to emotional contagion.

In succinct terms, the lifestyle and actions characteristic of a severely neurotic owner may contribute to the neuroses, anxious behavior, and aggressive behavior exhibited by a dog. General anxiety disorder is one of the most comorbid mental health conditions. General anxiety disorder frequently occurs concurrently with major depressive disorder, state anxiety disorders, and panic disorder.[10] There is also a strong association between generalized anxiety disorder and substance abuse disorder.[11]

One of the more significant human state anxieties relevant to the ontogenesis of a pet dog is social anxiety. Social anxiety disorder is characterized by persistent and marked fear/anxiety about one or more social or social performance situations.[12] Furthermore, the condition rarely occurs alone. 80% of persons with social anxiety disorder experience at least one other psychiatric disorder during their lifetime.[13]

Persons with social anxiety are more likely to avoid social contact with persons, neighborhood dogs, and many environmental contexts. Yet, early productive social exposure to people, dogs, and multifarious environments is vital to the emotional development of a young dog.

In an excellent experiment that observed the social behavior of mice, independent of pheromonal input, gonadal hormones, opponents, or social context, excitation of progesterone-receptor-expressing neurons in the ventromedial hypothalamus triggered territorial aggression in solitary male mice, but did not elicit territorial aggression in socially housed males, unless their pheromone-sensing was disabled.[14] Thus, of all the variables studied, upon exposure to the experimental stimulus, the only pertinent variable relevant to whether the mouse responded aggressively was whether the mouse was housed in a solitary manner or in a social environment. Hence, socialization is a key factor in the exhibition of territorially aggressive behavior in mice, and likely is the same for dogs.

In a study of 6,000 pet dogs, social fearfulness was associated with several factors, including poor socialization during puppyhood, infrequent participation in training, and infrequent activities.[15] Consequently, data supports that behaviors characteristic of persons with general anxiety or social anxiety, such as avoiding social contact and social activities, are likely to inhibit their dog’s emotional development in a manner that foments anxiety in the pet.

Anxiety certainly inhibits the quality of life of a pet, especially when contrasted to the quality of life expected from a more confident animal. Yet, from a societal standpoint what may be more calamitous is the relationship between anxiety, stranger-directed aggression, and dog-dog aggression.

The emotional state of an anxious owner may contagiously spread chronically or acutely to his/her dog.Photo Credit: Mark Spivak and Patricia King

Extrapolating further, when persons with general anxiety or social anxiety are exposed to social contexts they have an elevated probability of responding fearfully or even with panic. Unfortunately, in line with the principles of emotional contagion, their dogs may both chronically and acutely develop a mirrored response.

Domestic dogs have advanced abilities to respond to human behaviors or expectations.[16] Dogs may develop different strategies to handle challenging situations, based on the type of support they get from their owner.[17] When an owner is conveying an emotional message, dogs are capable of discerning between a happy or fearful expression and have some basic understanding that the emotional message refers to a specific object.[18] Dogs are skillful in acquiring information socially from humans and are able to copy the actions of a human demonstrator.[19]

Analyses of the data of English Cocker Spaniel owners revealed that owners of high aggression dogs were significantly more likely to be tense, emotionally less stable, shy, and undisciplined than owners of low aggression dogs.[20]

Resultantly, the anxiety or fear of an owner can readily be replicated by a dog and applied to the target of the owner’s acute anxiety.

Regardless, despite feeling fearful, few owners will want their dog to deliver a bite injury to an undeserving person or dog victim. Notwithstanding the anxious owner’s preferences, the dilemma is exacerbated by the probability that anxious people are less likely to enroll their dog in a training program and are intrinsically less capable of handling and managing their dog. Dogs owned by persons scoring high in neuroticism were less successful at operational tasks.[21] Yet, effective obedience may be essential to prevent a bite, especially once a dog progresses into a high-arousal state that may indicate impending or current aggression.

Moreover, the belief that anxious persons wish to avoid out of context bites is not true in all cases. A research study concluded persons lower in agreeableness and higher in neuroticism actively preferred a dog perceived as aggressive.[22] Perhaps the disagreeable anxious persons wish an aggressive dog for personal safety or perhaps to better enable social distance. Regardless, the presence of a neurotic owner increases the probability the dog will exhibit anxiety and associated aggression and that the owner will have reduced capability and maybe even reduced desire to properly control the animal.

IIb. Do Neurotic and Avoidant Owners Make Their Dogs Anxious?: Human Attachment Styles

John Bowlby, a British psychiatrist, psychologist, and psychoanalyst,[23]is credited as being the principal developer of attachment theory. Mary Ainsworth, an American-Canadian developmental psychologist, created the “strange-situation” test most frequently used by psychologists and researchers to measure attachment.[24]

Attachment theory is an enduring psychological connection with a meaningful person that forms pleasure responses and provides security in times of stress. The quality of attachment, most relevantly with a maternal figure, has a critical effect on emotional and social development, positive functioning, and psychological well-being.[25]

Infants undergo multiple stages of attachment with the primary initial attachment figure, whereupon they begin to also form bonds with additional caregivers, such as the father, older siblings, and grandparents. Attachment, which is highly valuable toward achieving healthy psychological development, depends upon the opportunity for attachment and quality caregiving. For instance, an infant separated from a maternal figure at birth and raised in an orphanage will likely have less opportunity to develop secure attachment than an infant raised in a typical maternal-child environment. Yet, not all maternal figures are quality caregivers who respond rapidly, reliably, and kindly to the infant’s emotional and physical needs.[26]

Bowlby described 4 primary attachment styles:

1) Secure attachment– occurs when the primary caregiver promptly, dependably, and sensitively provides physical and emotional comfort to the infant. The children tend to trust the caregiver, believe the caregiver will return to assist them, seek comfort from the caregiver as a secure base during times of stress, exhibit distress when separated from the caregiver, and exhibit pleasure upon the caregiver’s return. From an overall psychological standpoint, the children are frequently secure, happy, and wiling to explore environments.

2) Ambivalent attachment– occurs when the primary caregiver inconsistently and unreliably attends to the infant’s physical and emotional needs, where she is at times responsive and at other times neglectful. The attachment style may result from the parental style of interaction with the infant or from lack of schedule availability during times of need. The children tend to mistrust the caretaker, but feel severely distressed when the caretaker is absent and joyful upon the caretaker’s return. From an overall psychological standpoint, the children are disposed to anger, helplessness, passivity, and general insecurity.

3) Avoidant attachment– occurs when the primary caregiver is physically, emotionally, and/or operationally disengaged with the child or when the caregiver punishes or dismisses the child for seeking assistance or comfort from the caregiver. The attachment style may result from the parent being raised in a neglectful or abusive household. The children tend to avoid the caregiver and in the strange-situation test may show no preference between the caregiver or a stranger. From an overall psychological standpoint, the children are disposed to anxiety, lack of exploration, and general emotional distance.

4) Disorganized attachment– occurs when the primary caregiver inconsistently varies in response to the child. The disorganized parent may at times be responsive and at other times nonresponsive or erratically respond with passivity, aggression, or fear. The attachment style may result from similarly inconsistent treatment from parents. The children tend to avoid and resist the caregiver and exhibit disorientation and confusion. From an overall psychological standpoint, the children are disposed to depression, anger, passivity, and/or apathy.[27][28]

This enjoyable video provides a practical explanation of Bowlby’s attachment styles and their impact throughout a person’s social and emotional life:

Thus, the attachment style of a parent can have great effects on the personality development and associated behavior of a child. Given that the owner-dog relationship is tantamount to a parent child relationship, where the owner provides basic care, such as feeding and toileting, and also emotional care, such as praise, petting, proximity, and security, one should expect the attachment style of the owner to impact the emotional development and resultant behavior of the dog. Furthermore, we should expect that an owner exhibiting a secure attachment style will have the most psychological healthy and emotionally stable pet, whereas an owner exhibiting an avoidant or disorganized attachment style should have the most maladaptive and emotionally unstable pet. Research validates the preceding hypothesis.

Dogs behave similarly to children toward their mothers: owners are the preferred recipients of affiliative behaviors. Owners can present a secure base for their dogs.[29] There is evidence for an owner-specific secure base effect in dogs[30]

Dogs owned by “confident owners” were more likely to consider their owners as a “secure base” than were dogs owned by “non-confident owners.”[31] Dogs owned by confident owners applying a secure attachment pattern feel more secure when amidst the owner. Therefore, such dogs have a high probability of engaging calmly and proximally with the confident owner, rather than defending aggressively when the dog observes the approach of an interloper, in comparison to dogs owned by less confident owners or owners exhibiting less secure attachment patterns.

Dogs owned by persons considering them “social partners” and “meaningful companions” showed lower salivary cortisol levels than dogs owned by persons having a more distant relationship with their pets.[32] A lower level of salivary cortisol indicates a lower level of stress and a generally healthier animal, physically, physiologically, and psychologically.

The above footnoted statements document experiments confirming the benefits of secure owner-dog attachment. But what about insecure parent-child and owner-dog attachment styles?

Children of parents scoring high on attachment avoidance were more distressed during the inoculation than children of parents scoring low on avoidance.[33] With owners scoring higher on attachment-avoidance the occurrence of separation anxiety disorder increases. In addition, dogs scoring higher in the neuroticism scale were more prone to develop separation anxiety disorder. The results suggest that attachment avoidance may facilitate the development of separation anxiety in dogs.[34]

Pet avoidant attachment consists of feelings of discomfort with physical and emotional closeness. Persons with an avoidant attachment style maintain emotional distance from the pet, avoid intimacy with their pet, prevent the pet from intruding in their personal space, and exhibit difficulty in depending upon the pet and relying upon it when distressed.[35]

Persons scoring higher on pet attachment anxiety or avoidance were associated with less positive and more negative expectations about their pet’s availability and responsiveness. Pet owners who feel insecurely attached to their pet tend to view the pet as having negative or troubling characteristics, mistrust their pet’s intentions, and don’t expect the pet to be available, sensitive, and responsive to their needs.[36]

Persons who exhibit a neurotic and avoidant attachment style negatively impact the emotional state and behavior of their dog.Photo Credit: GRPH3B18Source: Wikimedia Commons

Furthermore, people who have an avoidant attachment style react differently upon the death of a pet. Whereas persons with an anxious personality type react with elevated distress, rumination, and loss of meaning of life, persons with an avoidant attachment style deactivate emotions.[37]

Compatible with the avoidant persons’ response to the death of a pet, persons who relinquish their dogs to shelters score lower on “companion animal attachment” than do continuing owners.[38]

Looking at data on animal abandonment:

• 45% of dogs abandoned to shelters are less than 1 year of age and 60% are less than 2 years of age.

• 59% of abandoned male dogs and 51% of abandoned female dogs are relinquished without a neuter or spay procedure, whereas in the general population only 14% of dogs are kept intact.[39]

• 22% of dogs are abandoned after less than 3 months of ownership, 49% after less than 1 year of ownership, and 62% after less than 2 years of ownership.

• 89% of persons abandoning a dog had paid less than $200 for the dog.

• 29% of abandoned dogs were characterized as “overly active” most or all of the time.

• 30% of the abandoned dogs were characterized as fearful at least some of the time.

• 16% of abandoned dogs growled, hissed, or snapped at least some of the time.

• 11% of abandoned dogs fought with other dogs.

• 12% of abandoned dogs had bitten a person.[40]

• 96% of abandoned dogs had not attended obedience classes or received professional training.[41]

• Abandoned dogs were less likely than continued dogs to receive veterinary care.

• Abandoned dogs were more likely than continued dogs to sleep outdoors.

• Abandoned dogs were more likely than continued dogs to be kept all day in a crate.[42]

In toto, persons who abandon their dogs are likely to maintain the relationship only for a short period; less likely to commit a substantial investment in the pet, for purchase, veterinary care, or training; more likely to keep their dog at a physical and emotional distance; and disproportionately likely to claim notable behavioral problems. The preceding is consistent with a caretaker avoidant attachment style and the developmental response to such a style.

Yet, the classic and most descriptive depiction of developmental maladaptation resulting from an avoidant attachment style is the series of cruel but enlightening rhesus macaque monkey experiments conducted by University of Wisconsin psychologist Harry Harlow. Harlow compared the personality and behavioral development of infant monkeys reared normally versus monkeys who experienced maternal deprivation, where their food sustenance and tactile contact was provided by surrogates made of cloth or wire. The monkeys raised by surrogates had a significantly higher probability of exhibiting reclusive behavior, social deficits, fear of exploration,[43]insecurity, fear, and aggressiveness.[44] Moreover, once immersed in a peer group, the surrogate-raised monkeys were more generally timid, unfamiliar with normal monkey social protocols, easily bullied by other monkeys, hesitant to mate, and inadequate mothers.[45] In addition, those raised exclusively by wire surrogates commonly experienced diarrhea.[46]

Moreover, the experiment showed that other than during brief periods of hunger tactile contact and the feeling of security were valued higher than was feeding. In addition, during an open field test, the presence of a tactile maternal source even if it was the cloth surrogate, increased exploratory behavior, whereas in the absence of the actual or surrogate caregiver the baby monkey was hesitant or afraid to explore, refused to move, and in the case of the surrogate-raised monkeys, often performed neurotic, compulsive thumb sucking. Furthermore, when frightened or startled by a novel object in the presence of the maternal figure, the young monkeys experienced less anxiety and either explored the object or sought the caregiver as a secure base.[47]

Fortunately, in the case of surrogate-raised monkeys less than 3 months of age, if they were immersed in a social group they could over time develop normal social skills and development, which indicates that if intervention occurs early enough another caregiver or social source can replace the developmental benefits typically provided by the mother. However, if immersion was delayed until after the critical period of development (3 months), then the social, emotional, and behavioral deficits usually remained permanent.[48][49]

Harlow also performed notable later experiments to study the effects of social isolation on the formation of depression. Isolated monkeys had worse social skills, insecurity in social situations, and a preference for separation from peers. More severely, social isolation resulted in catatonic behavior, anorexia, stereotypic behavior, and self-mutilation. The effects were often permanent, with the length of isolation having a great effect on the probability of modification once the monkey was immersed in a social group.[50]

Here is an excellent video of monkey responses in Harlow’s lab:

Later study provided a scientific explanation for Harlow’s experiments and the practical observations of attachment theory in humans and dogs. Touch during infancy reduces corticosteroid levels and increases the number of glucorticoid receptors in the central nervous system.[51] In contrast, protracted interruption of tactile contact reduces ornithine decarboxylase (ODC), which is necessary for cell growth and differentiation; diminishes growth hormone secretions; raises cortisol levels; lowers tissue responsiveness to ODC and growth hormone; weakens the immune system via a reduced ability to produce IgG and IgM antibodies;[52]and increases stress-induced activation of the hypothalamic-pituitary-adrenal axis.[53]

In summary, it should be clear how an avoidant owner has a higher probability of owning an anxious and aggressive dog.

III. Do Neurotic Dogs Make Their Owners Anxious?

In the prior section we confirmed that an anxious owner personality type or avoidant attachment style could predispose a dog to develop an anxious temperament or to exhibit aggressive behavior. However, is the phenomenon exclusively unidirectional, where the owner affects the dog, or is the process bidirectional, where the dog’s temperament and behavior can affect the owner? To answer the question we need first to determine whether dogs can be inherently anxious.

In a study of 13,700 Finnish pet dogs, there were large breed differences in the prevalence of all anxiety-related traits, suggesting a strong genetic contribution. Associatively, the researchers concluded that selective breeding focusing on behavior may reduce the prevalence of canine anxieties.[54]

In a study of 6,000 pet dogs, social fearfulness was associated with several factors, including urban environment, poor socialization during puppyhood, infrequent participation in training, infrequent activities, small body size, female gender, and neutering/spaying. In addition, the study identified several breed differences, suggesting a genetic contribution to social fearfulness.[55]

Moreover, there is a correlation between anxiety and the development of aggressive behavior. Sociability with humans correlated significantly negatively with child and stranger-directed aggression.[56] Dogs were more likely to demonstrate stranger-directed aggression if the participant rated them as mildly or severely fearful of strangers.[57]

Aggression toward unfamiliar dogs and people arises most commonly from fear and territoriality. A number of factors contribute to the development of aggression, including socialization deficits, hormones, genetics, and neurophysiologic components.[58]

A study of 17,000 dogs concluded that a large proportion of variance in dog behavior is attributable to genetic factors. Of the 14 behavioral traits studied the mean heritability was 0.51 +/- 0.12 SD. Traits with the highest heritability were trainability (0.73), stranger-directed aggression (0.68), and attachment and attention seeking (0.56).[59]

There is a high correlation between canine anxiety and aggressive behavior.Photo Credit: Mark Spivak

Combining the results from the preceding studies, dogs can be genotyped with a predisposition toward developing anxiety and aggression and fearful dogs are more predisposed toward developing aggressive behavior toward unfamiliar persons and dogs.

Moreover, experiments have shown that there are contexts that prompt innate anxiety and fear. When exposed to the predator scents of bear and lynx scat, a sample of 82 domestic dogs exhibited mean behavioral and biological responses indicating fear, whereas similar responses were not observed when the dogs were exposed to beaver scat or a non-sentient control odor.[60]

It is unlikely that the experimental dogs were previously exposed to any of the odors. Yet, they appeared to inherently respond fearfully to the predator odors, while not responding fearfully to the prey and control odors. Thus, anxiety and fear- and resultantly aggression- can have a strong genetic component.

More conspicuously, perhaps the most convincing experiments validating the genetic contribution to anxiety, fear, and aggression were the Belyaev fox experiments. Dmitry Belyaev was a Russian geneticist who in 1959 was quested with improving the production at silver fox farms, as fox fur was very popular in Russia.[61] Belyaev isolated 2 primary problems affecting the fox fur industry. First, aggressive foxes were difficult and dangerous to handle for the humans working on the farm. Second, stress reduced the animal’s breeding frequency and litter health. Therefore, Belyaev reasoned that if he selected animals for tameness and only bred the tame animals, then over generations they would be easier to handle and more prodigious in producing frequent litters, larger litters, and healthier puppies.[62]

Belyaev’s method of selection was remarkably simple. He stuck a gloved hand within each fox’s cage. The foxes that reacted aggressively were removed from the experiment, whereas the foxes that reacted least were selected for breeding. Within several generations both expected and unexpected outcomes occurred. Not only did Belyaev produce tame foxes that were calm and easy to handle, but the foxes changed in appearance and exhibited unanticipated behaviors.[63]

From an appearance standpoint, the foxes displayed spotted coats; floppy ears; curled tails; thicker limbs, and shorter, rounder muzzles. From a behavioral perspective they began behaving like domestic dogs. Instead of acting fearfully with humans, they followed humans, wagged tails when humans approached, licked the human caretakers, allowed humans to pick them up, and whined when humans departed.[64][65]

The experiment also found genetic anatomical and physiologically based causation for the foxes’ rapid evolution. Adrenal glands became progressively smaller; glucocorticoid (cortisol) levels reduced by half; and serotonin levels increased, which produced happier animals.[66] Resultantly, the foxes developed a less extreme hypothalamic-pituitary-adrenal response, which created calmer, less aggressive animals.[67]

Here is a video that provides an excellent visual and verbal account of Belyaev’s fox experiments:

Thus, it is incontrovertible that dogs can be born with genetically programmed tendencies to exhibit anxious and aggressive behavior. However, can an anxious dog create an anxious owner?

The answer lies in the principles of emotional contagion discussed in Section IIa. Emotional contagion fosters emotional synchrony between individuals, whereby a person or group influences the behavior of another person or group through the conscious or unconscious induction of emotional states and behavioral attitudes.[68][69] The phenomenon of emotional contagion has been found in humans, dogs, and primates. For instance, mob behavior in humans and predatory pack aggression in dogs are both examples of high-arousal emotional contagion.

Moreover, in line with the above human and dog examples, despite that fact that both positive and negative emotions can be contagious,[70]there are more behavioral indicators for arousal with negative valence states and sounds.[71] In addition, interspecies emotional communication can become contagious via olfactory chemosignals.[72][73]

Although more studies have focused on human to dog interspecies emotional communication, research has confirmed that the phenomenon is bidirectional. Furthermore, the innate human ability to recognize and respond to dog communication is improved via experience and a positive attitude toward the dog.[74]

The rate and extent of emotional convergence depends upon membership stability, mood regulation norms, task interdependence, and social interdependence.[75] Theories of coevolution between humans and dogs explain how humans became more adept at interpreting canine communication and more socially bonded with dogs as the species evolved from wolves into the many breeds of the contemporary domestic dog.

In an opinion piece in National Geographic, esteemed evolutionary anthropologist Brian Hare summarized dog-human coevolution. The following are excerpts from the article:[76]

• The wolf was domesticated at a time when humans were not very tolerant of carnivorous competitors.

• After modern humans arrived in Europe 43,000 years ago, they pretty much wiped out every large carnivore that existed.

• The success of dogs comes down to the survival of the friendliest.

• The wolves that were bold but aggressive were killed by humans. Only the ones that were bold and friendly were tolerated.

• Wolves approached us, probably while they were scavenging around garbage dumps at the edge of human settlements.

• This ability accounts for the extraordinary communication we have with our dogs.

• People who had dogs on a hunt would have an advantage over those who didn’t.

• Dogs also served as a warning system and a defense from hostile strangers and predators.

Therefore, domestication of the domestic dog prospered from humans’ abilities to interpret the emotional state of dogs (friendly vs. aggressive), intent and actions of dogs (locating prey by sight or scent), and communication of dogs (barking to alert of danger, barking or play bow to solicit play, solicitous look to indicate a need to urinate or eat).[77] In each of the preceding the dog learned to communicate purposefully and the human learned to respond accordingly.

Gaze-mediated bonding exists between dogs and humans. Mutual gazing increases oxytocin levels, which in turn increase affiliation and bonding. Human-like modes of communication, including mutual gaze, may have been acquired during the wolf to dog domestication process. Gazing behavior from dogs increases urinary oxytocin concentration in owners, which facilitates owner affiliation and subsequently increases oxytocin concentration in dogs. Findings support the existence of an interspecies oxytocin-mediated positive loop facilitated and modulated by gazing, which supports the coevolution of human-dog bonding by engaging common modes of communicating social attachment.[78]

Via selective breeding, humans accelerated an improved ability to interpret dog communication, actions, and emotions and to affiliate with dogs, whereby the dogs achieved superior utility as hunters, protectors, herders, and pets. The process was mutually advantageous. Moreover, in comparison to the wolves first domesticated 16,000 years ago, the contemporary domestic dog has greater membership stability, mood regulation norms, task interdependence, and social interdependence that facilitate contagious interspecies emotional interaction.

There is also a biological explanation for emotional contagion. Mirror neurons, which have been detected both in humans and monkeys, are visuomotor neurons within the brain’s premotor cortex that respond both when a particular action is performed by an individual and when the individual observes the same action performed by another. Mirror neurons form a cortical system matching observation and execution of goal-related motor actions. The function enables organisms to detect mental states of conspecifics that accord well with simulation theory.[79]

The simulation theory of empathy posits that capable organisms understand the behavior of others by activating mental processes that, if carried into action, would produce similar behavior. The concept includes intentional behavior, the expression of emotions, and the purposeful exhibition of emotions to project one’s emotional state onto others.[80] Thus, simulation theory explains our ability to comprehend and empathize with the emotional state and behavior of others and to intentionally affect the emotions and behavior of others.[81]

Frans de Waal, an acclaimed primatologist and ethologist, cites examples of simulation theory in multiple species, including dogs.[82] Moreover, the canine fMRI neuroscience research conducted by Berns and Spivak in Atlanta, GA and by the Miklosi Lab in Budapest, Hungary provide numerous examples of the similarities between the structure and function of dog and human brains. Therefore, it is not a stretch to assume that dogs also have mirror neurons and exhibit purposeful communication to affect the emotional state and behavior of others within their pack, be those pack members canine or human.

Would you rather handle a relaxed dog or an aggressive dog? Certainly, handling an aggressive dog can be nerve wracking, even for a normally calm person. Fortunately, this dog came to CPT for behavior modification training. If you read to the end you will see a behavioral metamorphosis after just one lesson.Photo Credit: Mark Spivak

Extrapolating further, both from a theoretical and practical perspective the probability is extremely high that a dog concerned by a stimulus could intentionally or inadvertently transmit an anxious emotional state to a human owner and perhaps even aggressive behavior to a human owner. From the standpoint of purposeful communication of emotions and behavior, an anxiously aggressive dog may wish its owner to align with it, which would strengthen the pack’s response to repel the stimulus. Moreover, given what we know about coevolution, emotional contagion, mirror neurons, and simulation theory of empathy, an owner predisposed to anxiety is likely to succumb to the dog’s intentions.

Yet, even when the human does not intentionally collaborate with the dog’s anxious emotional state and behavior, the human may inadvertently and undesirably share the dog’s anxiety. For instance, owners are generally consciously aware that if their dog inappropriately bites a human or dog the event poses legal, financial, and social detriment. Therefore, handling a difficult to manage, excitably anxious, fearfully anxious, or aggressively anxious dog is likely to invoke an anxious emotional state upon an owner concerned about potential liabilities.

For those interested learning more about emotional contagion and mirror neurons, you may wish to view this PBS video:

In summary, the evidence is strong that neurotic dogs can chronically and acutely create anxious owners.

Prior sections discussed how neurotic owners can create anxious dogs, how owners with an avoidant attachment style can create anxious dogs, and how anxious dogs can instigate owners to become acutely or chronically anxious. Consequently, primary anxiety on the part of one participant in the owner-dog relationship can foment secondary anxiety in the other participant.

But, what if both parties started anxious? Wouldn’t the likelihood be that anxiety in each would be magnified if both were primarily anxious and received a supplemental stimulus that also prompted secondary anxiety? Furthermore, the preceding would be a more frequent concern if neurotic owners exhibited a preference for purchasing or adopting anxious dogs.

Let’s begin answering the section header question by discussing theories of attraction. Theodore Newcomb, an American social psychologist, best known for his work while at Bennington College and the University of Michigan, formulated novel social attraction theories coined the Proximity Principle, Elaboration Principle, Similarity Principle, Complementary Principle, and Reciprocity Principle.[83][84]

The Proximity Principle states that persons tend to associate with, befriend, and be attracted to persons that are nearby. Newcomb explained the Proximity Principle as emanating from persons usually preferring what is familiar and the tendency for persons to have more frequent exposure repetition with those that reside proximally. Proximity fosters frequency, which promotes interaction, and resultantly increases the probability of a relationship.[85] In a sample group at Dartmouth College, geographic proximity and race were greater determinants of social interaction than were common interests, majors, or family background. However, despite disparity in race creating an obstacle to interaction, by placing persons of different races in proximal residences the likelihood of interaction increased threefold.[86] To apply the Proximity Principal to an owner-pet scenario, regardless of the temperament characteristics of the dog and owner, they are likely to bond with one another simply by residing together, provided one or both do not have a highly maladaptive temperament or attachment style.

The Elaboration Principle states that larger groups tend to form after members of dyads, triads, and small groups create relations with new persons they later merge into the existing group. Practical applications of the Elaboration Principle include gang recruitment, military recruitment, high school cliques, college fraternities, and college activity clubs.[87] The Elaboration Principle is pertinent to dog clubs or groups that meet at a dog park. Nevertheless, the Elaboration Principle is not highly relevant to the focus of our discussion.

The Similarity Principle states that persons tend to join groups that contain members who are similar to the person in values, attitudes, beliefs, races, gender, age, and other demographic factors.[88] Two conditions that promote interpersonal attraction between members of a dyad are perceived similarity of alter to self and interpersonal congruency.[89] The Similarity Principle is highly relevant to our discussion, as it set the groundwork for Morry’s Similar-Attraction Model.

The Complementary Principle states that in large groups the group will seek dissimilar members who productively complement existing members. For instance, a group of leaders will need followers and conversely a group of followers will need leaders.[90] Similarly, a group of introverted engineers starting a high-tech company will need an extraverted salesperson. The benefit of including complementary persons depends upon the flexibility of existing members. Complementarity and interpersonal rigidity were examined in relation to positive regard for others and group integration among 206 members of 54 musical bands. Complementarity was associated with more positive regard and more group integration in bands consisting of musicians who were high in interpersonal rigidity, whereas the effect was less strong in bands consisting of musicians who were lower in rigidity.[91] The Complementary Principle may apply in certain owner-dog dyads. For instance, an anxious, meek owner, who feels unsafe around people, may purposefully seek an aggressive animal to acquire a greater feeling of security and power.

The Reciprocity Principle states that persons are more apt to prefer and to engage in relationships with persons who accept them, respond favorably to them, and saliently like them.[92] The Reciprocity Principle is one of the primary reasons persons acquire a pet and have highly favorable opinions of their pet, as a pet often provides unconditional love that is less frequently observed in human-human contact.

There are many factors that lead to interpersonal attraction, including physical attraction, propinquity (frequency of proximal exposure), familiarity, similarity, complementarity, reciprocal liking, and reinforcement.[93]

Marian Morry, a psychology professor and head of the Close Relationship Laboratory at the University of Manitoba, expanded upon Newcomb’s work. Her lab examined how individual similarities and differences influence thoughts, feelings, and behaviors, related to the relationships a person has with friends and intimate partners.[94]

Most noteworthy, in 2005 Morry developed the attraction-similarity hypothesis. The attraction-similarity hypothesis predicts that in ongoing relationships projection of the self onto the other person is the result of the attraction. Therefore, satisfaction and attraction lead to perceptions of similarity.[95]

In same-sex friendships, the more satisfied people were with their friendships the more similar they perceived their friends to be to themselves.[96] Individuals often project their own attitudes, behaviors, or relationship views onto close others, which influences relationship judgments. College students believe their opposite-gender friends to be similar to themselves, although these beliefs may be a perception of the partner’s similarity, rather than an accurate assessment. Greater friendship satisfaction predicted greater perceived friend-self similarity.[97] Relationship quality and perceived similarity provide psychological benefits for the perceiver.[98]

North Americans show a significant pronounced similarity-attraction effect.[99] The crucial determinant of interactional satisfaction was neither the mood of the subject nor the mood of the partner, but their similarity in mood.[100] Actual security and self-security predicted attraction. With regard to perceptual factors, ideal similarity, self-similarity, and security all were significant predictors.[101] Similar attitudes relevant to the social context or interaction goals affect behavioral attraction and affective attraction.[102] The similarity-attraction effect is a well-known finding in human social psychology.[103] Individuals prefer mates similar to themselves.[104]

Here is an excellent video by the Khan Academy that explains Similarity-Attraction principles:

Thus, in accordance with Newcomb’s Similarity Principle and Morry’s Attraction-Similarity Model, people seek persons they believe are like themselves. In both platonic and intimate relationships perceptions of similarity correlate to superior relationship quality, and greater similarity psychologically benefits the participants in the relationship. However, the research presented thus far evaluated only human-human relationships. What about human-dog relationships?

The human-dog similarity-attraction research is more limited. Nevertheless, findings appear to indicate that relationship-seeking behavior in human-dog partnerships parallels the observations of Newcomb and Morry regarding human interpersonal attraction.

Owners reported more positive attitudes toward their pets when the behavioral style complemented their own interpersonal style.[105] The only dog characteristics to predict the dog-owner relationship were fearfulness and fear-related behavioral problems.[106]

In summary, people appear to apply the attraction-similarity hypothesis when selecting pets. Moreover, the effect may be more pronounced with anxious owners. I have a personal theory regarding why anxious owners tend to select anxious pets, even though cognitively they may realize there is a greater potential for detrimental outcomes.

In my opinion, the reason often is social self-validation. The Oxford dictionary definition of validation is “recognition or affirmation that a person or their feelings or opinions are valid or worthwhile.”[107] A person of low self-esteem is most likely to value validation. Saliently, low self-esteem is frequently comorbid with depression and anxiety.[108]

Consequently, anxious persons who question their worthiness purposefully select a dog mirroring their personality type. The selection fulfills a validation goal, as they consciously or unconsciously apply the logic, “If this dog is worthy of love, then so am I.”

The preceding hypothesis is in line with human-human similarity-attraction models, as one of the benefits of similar attraction espoused by social psychologists is the validation one receives by achieving acceptance from similar people. The video below entitled Similarity Attraction Theory describes the validation process:

Thus, in the past three sections we showed strong evidence that all three causations posited in Section I have relevance. However, should we just accept the inevitable? Or now that we have greater knowledge of owner-dog relationship dynamics is there something we can do to minimize problematic outcomes and incidences of dog-human and dog-dog aggression?

V. How Can CPT Address the Problem of Dog Anxiety and Aggression?

Relaxed dogs are rarely prone to aggressive behavior. In contrast, aroused dogs are more likely to exhibit aggressive behavior. Anxiety creates an aroused emotional state that predisposes a dog to a greater probability of manifesting out of context aggressive behavior. Moreover, such aggressive occurrences subject the owner to increased anxiety, a risk of cancellation of homeowner’s or renter’s insurance policies, animal control violations, civil financial liability, contempt from neighbors, conflicts with landlords and homeowners’ associations, and a reduction in enjoyment of the person’s pet owning experience.

In addition, a chronic anxiety condition is detrimental for the pet. Chronic stress reduces the pet’s physical and psychological health, spawns illnesses, and reduces lifespan.[109][110] More saliently, as supported in earlier sections and by 30 years of personal experience, owners are more likely to socially isolate an aggressive dog, less likely to walk the dog, and less likely to exercise the dog. Consequently, aggressive behavior causes the anxious-aggressive dog to suffer a diminished quality of life.

Fortunately, there are a number of preventive and treatment solutions CPT can provide dog owners.

1. Owner-Pet Matching

In accordance with the similarity attraction model, persons will fare best with a breed and individual dog that best matches his/her temperament and lifestyle, with the exception that anxious persons are better with confident, non-aggressive dogs versus anxious or anxiously aggressive dogs. Dependent upon an individual’s or family’s personality type, what breed is best? Should a person or family acquire a puppy, a young adult dog, or an adult dog?

The answer to both questions is, “It depends.” It depends upon the purchaser or adopter’s temperament, attachment style, schedule, residence, family composition, and lifestyle characteristics.

For an hourly fee, CPT consults with persons and families to assist them in matching their characteristics and desires to the optimal pet profile.

2. Litter and Dog Evaluations

Anatomical structure will usually remain fairly consistent within a breed, although it may vary somewhat between lines within a breed. For instance conformation English Labs will be thicker in the torso and have shorter legs in comparison to performance field-line Labrador Retrievers. Similarly, conformation German Shepherds will have increased angulation and a greater preponderance of black/tan saddle coats in comparison to working-line German Shepherds, which typically have a less angulated spine-hip structure and more frequent sable coats. Nevertheless, the structural and appearance differences won’t be so great that one believes the lineages are different breeds.

However, there may be great diversity in temperament within a breed, between lines, or even within a litter. Breeds will exhibit temperament and behavioral norms. Yet, the norms are only appropriate for the median member of the breed. There will be deviations from the norm, even significant deviations, within certain lines and specific individuals.

Therefore, once we identify the breed(s) displaying norms most appropriate for the client and determining whether the client is best acquiring a puppy, young adult, or adult dog, the next step is evaluating individual puppies within a litter or individual dogs available for adoption or sale. Evaluations maximize the probability that a selected candidate animal will be an optimal match for the client.

We believe CPT’s comprehensive evaluations are the best in the industry. They are a proprietary adaptation from existing validated evaluation protocols, information presented during scientific conferences and in research papers, and customized innovations created by CPT.

Some researchers have doubted the validity of litter evaluations and several influential persons with a political agenda have publicly doubted the accuracy of shelter dog evaluations. Nevertheless, our opinion is that well-designed, thorough evaluations executed by professional evaluators provide a high-degree of accuracy and certainly provide a higher probability of effective selection in comparison to the absence of information that would occur had the client never solicited a competent evaluation. Recent research tends to agree with CPT’s opinion.

Puppy tests can be a tool that provides early diagnosis of dogs genetically or phenotypically predisposed to developing aggressive behavior. Provided the test is valid and performed by an experienced professional, puppy tests can have substantial longitudinal consistency. Furthermore, there is no difference in personality consistency in dogs tested first as puppies and later as adults versus dogs tested again as puppies and later again as puppies. Moreover, aggression and submissiveness were the most consistent of the measured dimensions.[111]

Meta-analyses of the findings pertaining to inter-rater agreement, test-retest reliability, internal consistency, and convergent validity generally support the validity of canine temperament tests.[112]

Consequently, to obtain the highest probability of obtaining a puppy or dog of optimal temperament, aptitude, and structure, we highly recommend that anyone visiting a breeder, shelter, or rescue solicit a CPT professional evaluation prior to completing a purchase or adoption.

3. Housebreaking and Household Manners Training

Once the puppy or dog arrives at its new home, the first steps are teaching the dog to urinate and defecate outdoors, not indoors; to chew designated chew items, not furniture, carpet, trim, or sheetrock; to greet people by sitting, not by jumping; to remain quiet unless indicated, rather than to bark inappropriately and excessively; to play with toys, rather than to mouth family members; not to dig in the yard; not to climb on the furniture unless invited; to eat his/her own food, rather than to steal human food from the table or counters; and not to raid the trash or laundry basket.

CPT in-home private lessons are a terrific resource for teaching owners strategies how to prevent housebreaking and household manners problems or resolve existing problems. Similarly, a CPT board train is an excellent modality when owners prefer to delegate the work to CPT.

Training improves satisfaction with the animal, diminishes the likelihood of behavioral problems that produce dissatisfaction and/or emotional distance, and reduces the likelihood of rehoming. And from the standpoint of anxiety reduction, a trained dog is a happy dog and belongs to a happy owner.

4. Socialization Development Programs

As discussed in previous sections, early socialization is focal to preventing the formation of canine anxiety and aggression. Moreover, socialization should include interspecies (human, cat), intraspecies, and environmental exposures.

However, socialization is more complicated than simply having the dog meet people or dogs or taking the dog places. Not all socialization is productive socialization. Inopportune or inappropriate social exposures may be traumatic and highly counterproductive. Socialization programs need to be age appropriate and consider critical periods of emotional development, fear imprint periods, and the distinct temperament and behavior of the individual puppy or dog.

Via one or a combination of group class, private instruction, and/or board training CPT can design and implement a customized socialization development program that is optimized for each pet. Consequently, we maximize the probability of developing a confident, happy, healthy pet and a satisfied, bonded owner.

5. Leadership Communication Training

As discussed in previous sections, owner personality type and attachment style can affect the emotional development, emotional state, and behavior of the puppy or dog. Nevertheless, regardless of the owner’s or dog’s characteristics, once the owner learns to effectively administer human-dog leadership communication, then the owner will have greater impact in positively affecting the dog’s behavior, which includes greater control of potential aggressive propensities.

During private or in-home private consultations, CPT Head Trainers can instruct clients how to properly implement non-verbal and verbal communication that has the greatest impact in managing a dog’s behavior. Consequently, the owner can become an effective and benevolent leader that increases the dog’s confidence and reduces the likelihood of anxiety and undesirable aggressive behavior.

6. Spay/Neuter Information and Consultations

One of the questions, we frequently receive is, “Should I spay/neuter my pet?” Clients also frequently ask, “When should I spay neuter my pet?” The answers are not always simple.

CPT has authored a detailed article on the public policy history of spay/neuter surgery, modern changes in policy, international differences in policy, the potential negative and positive health effects of de-sexing a female or male dog, the negative and positive husbandry impact, and surgical and non-surgical options to spay/neuter. The article is heavily researched and includes over 40 footnoted original research studies. To access the article, entitled “Recent Research Raises Concerns Regarding Early Spaying/Neutering,” please click the link in this sentence.

In addition, since we wrote the referenced article, which focuses on the health and husbandry effects of surgical castration and ovariohysterectomy, researchers have released groundbreaking studies that question the assumed long-term behavioral benefits. It appears that both spaying and neutering increase the probability of a dog subsequently exhibiting aggressive behavior.

The phenomenon of spaying increasing the likelihood of aggression in female dogs was known previously, although most believed the effect insignificant. However, ethologists and veterinarians universally believed that neutering reduced the probability of aggression in male dogs. Yet, the newer research shows the previous belief may be true in the small minority of male dogs exhibiting true dominance aggression, but is false for the much larger number of male dogs exhibiting anxious temperaments, who frequently exhibit more pronounced anxiety and fear-aggression post a neuter surgery.

In an English study, neutered male dogs were 1.94x as likely to die prematurely, principally due to euthanasia after exhibiting behavioral problems, than were intact male dogs.[113] Multiple subsequent American studies replicated the results. Neutered males were more likely to be aggressive than any other group.[114]

The behavior of neutered dogs was significantly different from that of intact dogs in ways that contradict the prevailing view. Neutered dogs were more aggressive, fearful, excitable and less trainable than intact dogs. In addition, analysis revealed significant differences in bone growth between the intact and neutered groups. Moreover, the earlier the dog was neutered the more negative the effect on behavior and orthopedic development. These findings strongly support the need for an immediate re-evaluation of the current recommendation to spay or neuter dogs to prevent or treat behavioral problems, and an equally pressing need to more fully examine the wide range of physical effects of spaying and neutering pet dogs.[115]

There was a significant increase in the odds of moderate or severe aggression toward strangers for all gonadectomized dogs compared with intact dogs. Dogs gonadectomized between the ages of 7 – 12 months of age were 26% more likely to demonstrate aggression toward strangers. There is an urgent need to systematically examine other means of preventing unwanted procreation, such as vasectomy and hysterectomy.[116]

Given that recent research provides strong evidence that spaying and neutering may pose significant behavioral detriments, CPT advocates behavioral consultations to determine the pluses and minuses of gonadectomy surgery for a client pet, as it relates to the specific pet’s age, temperament, and behavior and the owner’s management style, lifestyle, and preferences. A CPT consultation can assist the owner in properly evaluating all major factors (health, husbandry, behavior) relevant to the decision whether to neuter/spay the dog and, if so, when.

CPT has no conflict of interest when assessing the relevant variables and presenting research information. Therefore, we highly recommend clients schedule a CPT consultation prior to committing their dog to a spay/neuter surgical procedure.

7. Behavior Modification Training

CPT behavior modification programs can do wonders in improving the emotional state and behavior of an anxious and/or aggressive dog. At the start of the appointment this dog was highly reactive to unfamiliar persons and dogs. However, after changes in leadership communication, some impulse control drills, improved leash walking mechanics, and several counterconditioning and systematic desensitization drills he can now behave calmly proximal to unfamiliar people and dogs. All this in just one lesson!Photo Credit: Mark Spivak

Numbers 1 – 7 in this Section are preventive. Prevention is optimal to minimize the probability of future problems. However, if a client first contacts CPT after a dog exhibits anxious traits or aggressive behavior or if prevention is insufficient, then treatment is indicated.

CPT Head Trainers specialize in scientific-based behavior modification training focused on human-dog communication, general impulse control, counterconditioning, and systematic desensitization principles. CPT’s protocols, usually administered via private and in-home private lessons, provide the highest probability of modifying general anxiety, state anxiety, and aggressive behavior. Consequently, the outcome produces less anxious pets, less anxious owners, and greater life satisfaction for both the human and animal.

VI. Conclusion

In summary, there is clearly a bidirectional relationship between owner and dog anxiety. A neurotic owner personality type and an avoidant owner attachment style can increase the probability of the pet developing anxiety and concomitant aggression. Likewise, an inherently anxious pet can negatively influence the owner to become chronically or acutely anxious. Furthermore, due to similarity-attraction principles, anxious owners are prone to acquiring anxious dogs, despite the fact that acquiring an anxious dog is more apt to lead to undesirable outcomes, including aggressive behavior.

Yet, there are a number of controllable factors, both from the standpoints of prevention and treatment, whereby CPT can decrease the probability of anxious and/or aggressive behavior or decrease the severity and resultant emotional and financial impact. Moreover, CPT’s involvement in preventive and treatment measures improves the human-animal bond, owner satisfaction of the pet owning experience, and the quality of life for both the owner and dog.

Persons interested in learning more about CPT’s training and behavior modification programs should review the Dog Training Brochure menu of www.cpt-training.com or contact CPT by phone at 404-236-2150.

[19]Fugazza C, Miklósi A. Should old dog trainers learn new tricks? The efficiency of the Do as I do method and shaping/clicker training method to train dogs. Appl Anim Behav Sci. 2014;153:53–61. [Google Scholar]

[39]Weiss, E; Gramann, S; Spain, CV; Slater, M. Goodbye to a Good Friend: An Explanation of the Re-homing of Cats and Dogs in the U.S. Research and Development, American Society for the Prevention of Cruelty to Animals. Oct 9, 2015. https://file.scirp.org/pdf/OJAS_2015100914300959.pdf

[42]Weiss, E; Gramann, S; Spain, CV; Slater, M. Goodbye to a Good Friend: An Explanation of the Re-homing of Cats and Dogs in the U.S. Research and Development, American Society for the Prevention of Cruelty to Animals. Oct 9, 2015. https://file.scirp.org/pdf/OJAS_2015100914300959.pdf